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Control of Blood Flow to Cardiac and Skeletal Muscle During Exercise

M. Harold Laughlin, Ronald J. Korthuis, Dirk J. Duncker, Robert J. Bache

10.1002/cphy.cp120116

Source: Supplement 29: Handbook of Physiology, Exercise: Regulation and Integration of Multiple Systems

Originally published: 1996

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Hemodynamics and Control of Blood Flow
1.1 Determinants of Vascular Resistance
1.2 Central Vascular Control Mechanisms
1.3 Local Vascular Control Mechanisms
2 Coronary Vascular Response to Exercise
2.1 Effect of Exercise on Left Ventricular Blood Flow
2.2 Right Ventricular Blood Flow during Exercise
2.3 Mechanisms Of Coronary Vasodilation during Exercise
2.4 Autonomic Nervous System Influences
2.5 Extravascular Determinants of Coronary Blood Flow
2.6 Epicardial Coronary Arteries
3 Effects of Physical Conditioning on the Coronary Circulation
3.1 Structural Adaptations
3.2 Adaptations of Neurohumoral Control
3.3 Local Coronary Vascular Control
3.4 Integrated Coronary Vascular Adaptations
3.5 Extravascular Determinants of Coronary Blood Flow
4 Skeletal Muscle Blood Flow During Exercise
4.1 Skeletal Muscle Blood Flow during Isometric Contraction
4.2 Skeletal Muscle Exercise Hyperemia
4.3 Regional Distribution of Skeletal Muscle Blood Flow
4.4 Mechanisms of Exercise Hyperemia
4.5 Regulation of Transcapillary Fluid and Solute Exchange in Skeletal Muscle
4.6 Regulation of Tissue Oxygenation in Exercising Skeletal Muscles
4.7 Determinants of Skeletal Muscle Arteriovenous Oxygen Difference
5 Effects of Physical Conditioning on Skeletal Muscle Vascular Beds
5.1 Skeletal Muscle Blood Flow Capacity
5.2 Skeletal Muscle Capillary Diffusion Capacity
5.3 Structural Vascular Adaptation
5.4 Adaptations of Vascular Control
6 Conclusion
Figure 1. Figure 1.

Relationship between blood flow and exercise intensity in skeletal muscles of different fiber‐type composition in rats and miniature swine. A, Data for the red (VLR) and white (VLW) portions of the vastus lateralis muscle and the soleus muscle (S) for rat skeletal muscles are shown on the left. The percentage fiber‐type compositions for these muscle are: VLR = 2% SO (slow‐twitch, oxidative), 64% FOG (fast‐twitch, oxidative, glycolytic), 34% FG (fast‐twitch, glycolytic); VLW = 0% SO, 1% FOG, 99% FG; S = 77% SO, 23% FOG, 0% FG 311. Rest data are from Laughlin and Armstrong 310 for anesthetized rats. PE = preexercise (i.e. data collected with the animals standing on the treadmill involved in normal activity). PE data and data for rats running on the treadmill at speeds of 15–105 m/min are from Laughlin and Armstrong 311 and Armstrong and Laughlin 25. B, Data for the medial head (MH) and the deep (LHR) and superficial (LHW) portions of the long head of triceps brachii muscles of miniature swine are presented on the right. The percentage fiber‐type compositions for these muscles are: LHR = 46% SO, 43% FOG, 12% FG; LHW = 8% SO, 38% FOG, 54% FG; MH = 91% SO, 9% FOG, 0% SO.

Rest data are unpublished observations from anesthetized pigs. PE data and data for pigs running on a treadmill at speeds of 4.8–17.7 km/h are from Armstrong et al. was demonstrated at a running speed of 14.5 km/h in these pigs 20
Figure 2. Figure 2.

Myocardial oxygen balance in awake dogs at rest and during four incremental levels of treadmill exercise. The increase in myocardial oxygen consumption was for the most part accommodated for by an increase in coronary blood flow with only modest contributions of increases in hematocrit and oxygen extraction. MVO2, myocardial oxygen consumption; Hct, hematocrit; Art O2 sat, arterial oxygen saturation; CVO2 sat = coronary venous oxygen saturation. Data are mean SEM, and are from von Restorff et al. 557.
Figure 3. Figure 3.

Relationship between heart rate (HR) and left ventricular myocardial blood flow (LVMBF) at rest and during treadmill exercise in fogs 37,38,43,46,53,406,557, swing 75,76,136,318,393,460,461,568, horses 22,350,410, and humans 150,217,236,266,268,278,392,433.
Figure 4. Figure 4.

Distribution of cardiac output to skeletal muscle (muscle), heart, visceral organs, and other tissues of miniature swine as a function of oxygen consumption, over the full range of oxygen uptake from rest to . Data are from Armstrong et al. 20. Note that blood flow to the heart and skeletal muscle increases with increases in exercise intensity, whereas visceral blood flows decrease.
Figure 5. Figure 5.

Relationship between heart rate and coronary blood flow at rest and during four incremental levels of treadmill exercise in dogs, under control conditions (Control, open circles), during channel blockade (glibenclamide, 50 μg · kg−1 · min−1, intracoronary) (Glib, open squares), and during combined adenosine receptor blockade (8‐phenyltheophylline, 5 mg/kg intravenously) and channel blockade (Glib+8PT, closed squares). channel blockade alone decreased coronary blood flow at rest but did not affect the exercise‐induced increase in coronary flow. In contrast, combined adenosine receptor and KATP + channel blockade decreased coronary blood flow at rest and markedly attenuated the increase in coronary flow produced by exercise. Data are mean ± SEM, n = 11. Data are from Duncker et al. 139.
Figure 6. Figure 6.

Effects of exercise training on the myocardial oxygen balance in awake dogs at rest and during four incremental levels of treadmill exercise. A, Exercise training had no effect on the arterial oxygen‐carrying capacity, but caused a small but significant increase in myocardial oxygen extraction and decreased coronary blood flow at comparable workloads during exercise (reflected by total‐body oxygen consumption. B, However, the relationship between myocardial oxygen consumption and coronary blood flow was not altered by exercise training, as the increase in myocardial oxygen extraction was too small to result in a measurable decrease in coronary blood flow. Body , total body oxygen consumption; MVO2, myocardial oxygen consumption; Hct, hematocrit; Art O2 sat, arterial oxygen saturation; CVO2 sat, coronary venous oxygen saturation. Data are mean ± SEM, and are from von Restorff et al. 557.
Figure 7. Figure 7.

Hemodynamic effects of rhythmic, 0.2 ms duration, tetanic contractions of cat calf muscle at a frequency of one tetanic contraction per second. Femoral venous pressure was increased to 50 mm Hg by elevations of outflow catheter as described by Folkow et al. 169.

Adapted from Folkow et al. 169
Figure 8. Figure 8.

Effects of frequency of contraction on vascular conductance of the dog hind limb. Data from Sheriff et al. 495. Note that doubling contraction frequency by increasing treadmill speed from 2 mph to 4 mph at 0% grade resulted in the initial rise in conductance to approximately double. In contrast, when the treadmill grade was increased from 0% to 10% and running speed held the same at 4 mph, the initial increase in vascular conductance is similar. Finally, note that the steady‐state vascular conductance (15–30 s) appeared to be related to metabolic rate under all three conditions. These results were obtained from dogs in which cardiovascular reflex responses were blocked with hexamethonium (10 mg/kg, intravenously), atropine (0.2 mg/kg, intravenously), and captopril (1 mg/kg, intravenously) and during AV‐linked ventricular pacing as described in Sheriff et al. 495.
Figure 9. Figure 9.

Apparent vascular conductance and blood flows of rat skeletal muscle.

Adapted from Laughlin 304.] Vascular conductance was calculated for perfusion pressures of 130 mm Hg with equations derived from linear regression analysis of conductance (for each muscle) and perfusion pressure (corrected for effects of viscosity). Data for resting conditions are from Laughlin and Ripperger 325, data for twitch and tetanic conditions are from Mackie and Terjung 346, and data for running rats are from Armstrong and Laughlin 25. Data for twitch contractions were collected after 10 min of contraction and for tetanic contractions after 1 min of contractions
Figure 10. Figure 10.

Blood flow to rat skeletal muscles as a function of time during high‐intensity treadmill exercise. Rats ran at 60 m/min from time 0 through 3 min. Recovery blood flows were measured at 30 s and 3 min following exercise. Data are presented for red (triangles) and white (boxes) vastus lateralis, biceps femoris (open circles), and total hindlimb muscle (filled circles).

Adapted from Armstrong and Laughlin 23
Figure 11. Figure 11.

Overview of changes in autonomic control of the cardiovascular system associated with increase intensity in humans. At rest, vagal control is important. Sympathetic nervous activity starts to increase as vagal control is withdrawn. Vagal control is negligible and sympathetic activity beginning to increase when exercise intensity produces heart rates of about 100 bpm. Indices of increased sympathetic nervous activity include: decreases in blood flow to splanchnic (SBF) and renal (RBF) vascular beds, increased plasma norepinephrine (NE) concentrations, increased plasma renin activity (PRA), and increased muscle sympathetic nerve activity (MSNA). Blood lactate concentration (HLa) does not increase until exercise intensity is 50%–60% of (Heart rates of 130–140 bpm).

Adapted from Rowell et al. 449


Figure 1.

Relationship between blood flow and exercise intensity in skeletal muscles of different fiber‐type composition in rats and miniature swine. A, Data for the red (VLR) and white (VLW) portions of the vastus lateralis muscle and the soleus muscle (S) for rat skeletal muscles are shown on the left. The percentage fiber‐type compositions for these muscle are: VLR = 2% SO (slow‐twitch, oxidative), 64% FOG (fast‐twitch, oxidative, glycolytic), 34% FG (fast‐twitch, glycolytic); VLW = 0% SO, 1% FOG, 99% FG; S = 77% SO, 23% FOG, 0% FG 311. Rest data are from Laughlin and Armstrong 310 for anesthetized rats. PE = preexercise (i.e. data collected with the animals standing on the treadmill involved in normal activity). PE data and data for rats running on the treadmill at speeds of 15–105 m/min are from Laughlin and Armstrong 311 and Armstrong and Laughlin 25. B, Data for the medial head (MH) and the deep (LHR) and superficial (LHW) portions of the long head of triceps brachii muscles of miniature swine are presented on the right. The percentage fiber‐type compositions for these muscles are: LHR = 46% SO, 43% FOG, 12% FG; LHW = 8% SO, 38% FOG, 54% FG; MH = 91% SO, 9% FOG, 0% SO.

Rest data are unpublished observations from anesthetized pigs. PE data and data for pigs running on a treadmill at speeds of 4.8–17.7 km/h are from Armstrong et al. was demonstrated at a running speed of 14.5 km/h in these pigs 20


Figure 2.

Myocardial oxygen balance in awake dogs at rest and during four incremental levels of treadmill exercise. The increase in myocardial oxygen consumption was for the most part accommodated for by an increase in coronary blood flow with only modest contributions of increases in hematocrit and oxygen extraction. MVO2, myocardial oxygen consumption; Hct, hematocrit; Art O2 sat, arterial oxygen saturation; CVO2 sat = coronary venous oxygen saturation. Data are mean SEM, and are from von Restorff et al. 557.



Figure 3.

Relationship between heart rate (HR) and left ventricular myocardial blood flow (LVMBF) at rest and during treadmill exercise in fogs 37,38,43,46,53,406,557, swing 75,76,136,318,393,460,461,568, horses 22,350,410, and humans 150,217,236,266,268,278,392,433.



Figure 4.

Distribution of cardiac output to skeletal muscle (muscle), heart, visceral organs, and other tissues of miniature swine as a function of oxygen consumption, over the full range of oxygen uptake from rest to . Data are from Armstrong et al. 20. Note that blood flow to the heart and skeletal muscle increases with increases in exercise intensity, whereas visceral blood flows decrease.



Figure 5.

Relationship between heart rate and coronary blood flow at rest and during four incremental levels of treadmill exercise in dogs, under control conditions (Control, open circles), during channel blockade (glibenclamide, 50 μg · kg−1 · min−1, intracoronary) (Glib, open squares), and during combined adenosine receptor blockade (8‐phenyltheophylline, 5 mg/kg intravenously) and channel blockade (Glib+8PT, closed squares). channel blockade alone decreased coronary blood flow at rest but did not affect the exercise‐induced increase in coronary flow. In contrast, combined adenosine receptor and KATP + channel blockade decreased coronary blood flow at rest and markedly attenuated the increase in coronary flow produced by exercise. Data are mean ± SEM, n = 11. Data are from Duncker et al. 139.



Figure 6.

Effects of exercise training on the myocardial oxygen balance in awake dogs at rest and during four incremental levels of treadmill exercise. A, Exercise training had no effect on the arterial oxygen‐carrying capacity, but caused a small but significant increase in myocardial oxygen extraction and decreased coronary blood flow at comparable workloads during exercise (reflected by total‐body oxygen consumption. B, However, the relationship between myocardial oxygen consumption and coronary blood flow was not altered by exercise training, as the increase in myocardial oxygen extraction was too small to result in a measurable decrease in coronary blood flow. Body , total body oxygen consumption; MVO2, myocardial oxygen consumption; Hct, hematocrit; Art O2 sat, arterial oxygen saturation; CVO2 sat, coronary venous oxygen saturation. Data are mean ± SEM, and are from von Restorff et al. 557.



Figure 7.

Hemodynamic effects of rhythmic, 0.2 ms duration, tetanic contractions of cat calf muscle at a frequency of one tetanic contraction per second. Femoral venous pressure was increased to 50 mm Hg by elevations of outflow catheter as described by Folkow et al. 169.

Adapted from Folkow et al. 169


Figure 8.

Effects of frequency of contraction on vascular conductance of the dog hind limb. Data from Sheriff et al. 495. Note that doubling contraction frequency by increasing treadmill speed from 2 mph to 4 mph at 0% grade resulted in the initial rise in conductance to approximately double. In contrast, when the treadmill grade was increased from 0% to 10% and running speed held the same at 4 mph, the initial increase in vascular conductance is similar. Finally, note that the steady‐state vascular conductance (15–30 s) appeared to be related to metabolic rate under all three conditions. These results were obtained from dogs in which cardiovascular reflex responses were blocked with hexamethonium (10 mg/kg, intravenously), atropine (0.2 mg/kg, intravenously), and captopril (1 mg/kg, intravenously) and during AV‐linked ventricular pacing as described in Sheriff et al. 495.



Figure 9.

Apparent vascular conductance and blood flows of rat skeletal muscle.

Adapted from Laughlin 304.] Vascular conductance was calculated for perfusion pressures of 130 mm Hg with equations derived from linear regression analysis of conductance (for each muscle) and perfusion pressure (corrected for effects of viscosity). Data for resting conditions are from Laughlin and Ripperger 325, data for twitch and tetanic conditions are from Mackie and Terjung 346, and data for running rats are from Armstrong and Laughlin 25. Data for twitch contractions were collected after 10 min of contraction and for tetanic contractions after 1 min of contractions


Figure 10.

Blood flow to rat skeletal muscles as a function of time during high‐intensity treadmill exercise. Rats ran at 60 m/min from time 0 through 3 min. Recovery blood flows were measured at 30 s and 3 min following exercise. Data are presented for red (triangles) and white (boxes) vastus lateralis, biceps femoris (open circles), and total hindlimb muscle (filled circles).

Adapted from Armstrong and Laughlin 23


Figure 11.

Overview of changes in autonomic control of the cardiovascular system associated with increase intensity in humans. At rest, vagal control is important. Sympathetic nervous activity starts to increase as vagal control is withdrawn. Vagal control is negligible and sympathetic activity beginning to increase when exercise intensity produces heart rates of about 100 bpm. Indices of increased sympathetic nervous activity include: decreases in blood flow to splanchnic (SBF) and renal (RBF) vascular beds, increased plasma norepinephrine (NE) concentrations, increased plasma renin activity (PRA), and increased muscle sympathetic nerve activity (MSNA). Blood lactate concentration (HLa) does not increase until exercise intensity is 50%–60% of (Heart rates of 130–140 bpm).

Adapted from Rowell et al. 449
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Article Title: Control of Blood Flow to Cardiac and Skeletal Muscle During Exercise
 

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M. Harold Laughlin, Ronald J. Korthuis, Dirk J. Duncker, Robert J. Bache. Control of Blood Flow to Cardiac and Skeletal Muscle During Exercise. Compr Physiol 2011, Supplement 29: Handbook of Physiology, Exercise: Regulation and Integration of Multiple Systems: 705-769. First published in print 1996. doi: 10.1002/cphy.cp120116